Prenatal programming of depression and schizophrenia?

Neuroembryology

Volumn 1, Issue 3, 2002, Pages 113-127

  Dafotakis, Manuel ^a   Vehoff, Jochen ^a   Korr, Hubert ^a   Schmitz, Christoph ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Autoradiography; Prenatal irradiation; Prenatal stress; Stereology

Indexed keywords

BRAIN DEVELOPMENT; DEPRESSION; LABORATORY; MEDICAL LITERATURE; NONHUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; PROPHYLAXIS; REGULATORY MECHANISM; REVIEW; SCHIZOPHRENIA; X IRRADIATION;

ANIMALIA;

EID: 0344708484     PISSN: 14248522     EISSN: None     Source Type: Journal    
DOI: 10.1159/000063531     Document Type: Review

References (217)

1. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS: Fetal nutrition and cardiovascular disease in adult life. Lancet 1993;341:938-941.
2. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM: Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): Relation to reduced fetal growth. Diabetologia 1993;36:62-67.
3. Barker DJ, Godfrey KM, Fall C, Osmond C, Winter PD, Shaheen SO: Relation of birth weight and childhood respiratory infection to adult lung function and death from chronic obstructive airways disease. BMJ 1991;303:671-675.
4. Cresswell JL, Barker DJ, Osmond C, Egger P, Phillips DI, Fraser RB: Fetal growth, length of gestation, and polycystic ovaries in adult life. Lancet 1997;350:1131-1135.
5. Godfrey KM, Barker DJ, Osmond C: Disproportionate fetal growth and raised IgE concentration in adult life. Clin Exp Allergy 1994;24:641-648.
6. Barker DJ, Osmond C: Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986;334:1077-1081.
7. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ: Weight in infancy and death from ischaemic heart disease. Lancet 1989;337:577-580.
8. Barker DJ: Rise and fall of Western diseases. Nature 1989;338:371-372.
9. Watson JB, Mednick SA, Huttunen M, Wang X: Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 1999;11:457-466.
10. Susser ES, Schaefer CA, Brown AS, Begg MD, Wyatt RJ: The design of the prenatal determinants of schizophrenia study. Schizophr Bull 2000;26:257-273.
11. Chan WY, Kostovic I, Takashima S, Feldhaus C, Stoltenburg-Didinger G, Verney C, Yew D, Ulfig N: Normal and abnormal development of the human cerebral cortex. Neuroembryology 2002;1:78-90.
12. Godfrey KM, Barker DJ: Fetal nutrition and adult disease. Am J Clin Nutr 2000;71:1344S-1352S.
13. Alonso SJ, Castellano MA, Quintero M, Navarro E: Action of antidepressant drugs on maternal stress-induced hypoactivity in female rats. Methods Find Exp Clin Pharmacol 1999;21:291-295.
14. Dugovic C, Maccari S, Weibel L, Turek FW, Van Reeth O: High corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J Neurosci 1999;19:8656-8664.
15. Lyon M, McClure WO: Investigations of fetal development models for prenatal drug exposure and schizophrenia. Prenatal d-amphetamine effects upon early and late juvenile behavior in the rat. Psychopharmacology 1994;116:226-236.
16. Fiore M, Talamini L, Angelucci F, Koch T, Aloe L, Korf J: Prenatal methylazoxymethanol acetate alters behavior and brain NGF levels in young rats: A possible correlation with the development of schizophrenia-like deficits. Neuropharmacology 1999;38:857-869.
17. Shalev U, Weiner I: Gender-dependent differences in latent inhibition following prenatal stress and corticosterone administration. Behav Brain Res 2001;126:57-63.
18. Yadid G, Nakash R, Deri I, Tamar G, Kinor N, Gispan I, Zangen A: Elucidation of the neurobiology of depression: Insights from a novel genetic animal model. Prog Neurobiol 2000;62:353-378.
19. Redei EE, Ahmadiyeh N, Baum AE, Sasso DA, Slone JL, Solberg LC, Will CC, Volenec A: Novel animal models of affective disorders. Semin Clin Neuropsychiatry 2001;6:43-67.
20. Ellenbroek BA, Cools AR: Animal models with construct validity for schizophrenia. Behav Pharmacol 1990;1:469-490.
21. Swerdlow NR, Geyer MA: Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 1998;24:285-301.
22. Hornig M, Lipkin WI: Infectious and immune factors in the pathogenesis of neurodevelopmental disorders: Epidemiology, hypotheses, and animal models. Ment Retard Dev Disabil Res Rev 2001;7:200-210.
23. Weinstock M, Fride E, Hertzberg R: Prenatal stress effects on functional development of the offspring. Prog Brain Res 1988;73:319-331.
24. Weinstock M: Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci Biobehav Rev 1997;21:1-10.
25. Weinstock M: Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 2001;65:427-451.
26. Stott DH: Follow-up study from birth of the effects of prenatal stresses. Dev Med Child Neurol 1973;5:770-787.
27. Meijer A: Child psychiatric sequelae of maternal war stress. Acta Psychiatr Scand 1985;72:505-511.
28. Zappitelli M, Pinto T, Grizenko N: Pre-, peri-, and postnatal trauma in subjects with attention-deficit hyperactivity disorder. Can J Psychiatry 2001;46:542-548.
29. Alonso SJ, Arevalo R, Afonso D, Rodriguez M: Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring. Physiol Behav 1991;50:511-517.
30. Pellow S, File SE: Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus maze: A novel test of anxiety in the rat. Pharmacol Biochem Behav 1986;24:525-529.
31. Fride E, Weinstock M: Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci 1988;42:1059-1065.
32. Wakshlak A, Weinstock M: Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol Behav 1990;48:289-292.
33. Poltyrev T, Keshet GI, Kay G, Weinstock M: Role of experimental conditions in determining differences in exploratory behavior of prenatally stressed rats. Dev Psychobiol 1996;29:453-462.
34. Shell LM: Environmental noise and human prenatal growth. Am J Physiol Anthropol 1981;56:63-70.
35. 14C-4- corticosterone from the rat mother to the foetus and neonate. Nature 1970;226:1058-1059.
36. Guillemin R, Vargo T, Rossier J, Minick S, Ling N, Rivier C, Vale W, Bloom F: β-Endorphin and adrenocorticotropin are selected concomitantly by the pituitary gland. Science 1977;197:1367-1369.
37. Sandman CA, Kastin AJ: The influence of fragments of the LPH chains on learning, memory and attention in animals and man. Pharmacol Ther 1981;13:39-60.
38. Falconer J, Chan EC, Madsen G, Thomson M, Davies J, Smith R: Secretion of beta-endorphin into the maternal circulation by uteroplacental tissues in response to hypoglycaemic stress. J Endocrinol 1988;118:R5-R8.
39. Joffe JM: Prenatal Determinants of Behavior. Oxford, Pergamon, 1969.
40. Joffe JM: Hormonal mediation of the effects of prenatal stress on offspring behavior; in Gottlieb G (ed): Studies on the Development of Behavior and the Nervous System: Early Influences. New York, Academic Press, 1978, vol 4, pp 108-144.
41. Cratty MS, Ward HE, Johnson EA, Azzaro AJ, Birkle DL: Prenatal stress increases corticotro-pin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res 1995;675: 297-302.
42. Day JC, Koehl M, Deroche V, Le Moal M, Maccari S: Prenatal stress enhances stress- and corticotropin-releasing factor-induced stimulation of hippocampal acetylcholine release in adult rats. J Neurosci 1998;18:1886-1892.
43. Weinstock M, Matlina E, Maor GI, Rosen H, McEwen BS: Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary-adrenal system in the female rat. Brain Res 1992;595:195-200.
44. Ohkawa T, Takeshita S, Murase T, Okinaga S, Arai K: The effect of an acute stress in late pregnancy on hypothalamic catecholamines of the rat fetus. Nippon Sanka Fujinka Gakkai Zasshi 1991;43:783-787.
45. Epstein MF, Farrell PM, Sparks JW, Pepe G, Driscoll SG, Chez RA: Maternal betamethasone and fetal growth and development in the monkey. Am J Obstet Gynecol 1977;127:261-263.
46. Reinisch JM, Simon NG, Karow WG, Gandelman R: Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 1978;202:436-438.
47. Uno H, Lohmiller L, Thieme C, Kemnitz JW, Engle MJ, Roecker EB, Farrell PM: Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Dev Brain Res 1990;53:157-167.
48. Matsumoto A, Arai Y: Sexual differentiation of neuronal circuitry in the neuroendocrine hypothalamus. Biomed Rev 1997;7:5-15.
49. McCormick CM, Smythe JW, Sharma S, Meaney MJ: Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Dev Brain Res 1995;84:55-61.
50. Peters DAV: Prenatal stress: Effects on brain biogenic amine and plasma corticosterone levels. Pharmacol Biochem Behav 1982;17:721-726.
51. Fride E, Dan Y, Feldon J, Halevy G, Weinstock M: Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 1986;37:681-687.
52. Takahashi LK, Kalin NH: Early developmental and temporal characteristics of stress-induced secretion of pituitary-adrenal hormones in prenatally-stressed rat pups. Brain Res 1991;558:75-78.
53. Clarke AS, Schneider ML: Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev Psychobiol 1993;26:293-304.
54. Clarke AS, Wittwer DJ, Abbott DH, Schneider ML: Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev Psychobiol 1994;27:257-269.
55. Takahashi LK: Prenatal stress: Consequences of glucocorticoids on hippocampal development and function. Int J Dev Neurosci 1998; 16:199-207.
56. Ward HE, Johnson EA, Salm AK, Birkle DL: Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol Behav 2000;70:359-366.
57. Henry C, Kabbaj M, Simon H, Le Moal M, Maccari S: Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 1994; 6:341-345.
58. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M: Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 1995;15:110-116.
59. Kay G, Tarcic N, Poltyrev T, Weinstock M: Prenatal stress depresses immune function in rats. Physiol Behav 1998;63:397-402.
60. Fameli M, Kitraki E, Stylianopoulou F: Effects of hyperactivity of the maternal hypothalamic-pituitary-adrenal (HPA) axis during pregnancy on the development of the HPA axis and brain monoamines of the offspring. Int J Dev Neurosci 1994;12:651-659.
61. Frye CA, Bayon LE: Prenatal stress reduces the effectiveness of the neurosteroid 3 alpha, 5 alpha-THP to block kainic-acid-induced seizures. Dev Psychobiol 1999;34:227-234.
62. Koehl M, Darnaudery M, Dulluc J, Van Reeth O, Le Moal M, Maccari S: Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 1999;40:302-315.
63. Barbazanges A, Piazza PV, Le Moal M, Maccari S: Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 1996;16:3943-3949.
64. Vallée M, Mayo W, Maccari S, Le Moal M, Simon H: Long-term effects of prenatal stress and handling on metabolic parameters: Relationship to corticosterone secretion response. Brain Res 1996;18:287-292.
65. Vallée M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S: Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: Correlation with stress-induced corticosterone injection. J Neurosci 1997;17:2626-2636.
66. Stohr T, Schulte Wermeling D, Szuran T, Pliska V, Domeney A, Welzl H, Weiner I, Feldon J: Differential effects of prenatal stress in two inbred strains of rats. Pharmacol Biochem Behav 1998;59:799-805.
67. Fride E, Dan Y, Gavish M, Weinstock M: Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors. Life Sci 1985;36:2103-2109.
68. Beaulieu S, Gagné B, Barden N: Glucocorticoid regulation of proopiomelanocortin messenger ribonucleic acid content of rat hypothalamus. Mol Endocrinol 1988;2:727-731.
69. Ferrarese C, Appolonio I, Biachi G, Frigo M, Marzorati C, Pecora N, Perego M, Pierpaoli C, Frattola L: Benzodiazepine receptors and diazepam binding inhibitor: A possible link between stress, anxiety and the immune system. Psychoneuroendocrinology 1993;18:3-22.
70. Insel TR, Kinsley CH, Mann PE, Bridges RS: Prenatal stress has long-term effects on brain opiate receptors. Brain Res 1990;511:93-97.
71. Siegel RA, Chowers I, Conforty N, Feldman S, Weidenfeld J: Effects of naloxone on basal and stress-induced ACTH and corticosterone secretion in the male rat - Site and mechanism of action. Brain Res 1982;249:103-109.
72. Odio M, Brodish A: Central but not peripheral opiate receptor blockade prolonged pituitary-adrenal resposes to stress. Physiol Biochem Behav 1990;35:963-969.
73. Jacobson L, Sapolsky R: The role of the hippocampus in the feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 1991;12:118-134.
74. Herman JP, Cullinan WE: Neurocircuitry of stress: Central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997;20:78-84.
75. Feldman S, Weidenfeld J: The excitatory effects of the amygdala on hypothalamo-pituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res Bull 1998;45:389-393.
76. Feldman S, Newman ME, Gur E, Weidenfeld J: Role of serotonin in the amygdala in hypothalamo-pituitary-adrenocortical responses. Neuroreport 1998;9:2007-2009.
77. Peters DAV: Maternal stress increases fetal brain and neonatal cerebral cortex 5-hydroxy-tryptamine synthesis in rats: A possible mechanism by which stress influences brain development. Pharmacol Biochem Behav 1990;35: 943-947.
78. Huttenen MO, Niskanen P: Persistent alteration of turnover of brain noradrenaline in the offspring of rats subjected to stress during pregnancy. Nature 1971;230:53-55.
79. Weiss JM, Goodman PA, Losito BG, Corrigan S, Charry JM, Bailey WH: Behavioral depression produced by an uncontrollable stressor: Relationship to norepinephrine, dopamine and serotonin levels in various regions of the rat brain. Brain Res Rev 1981;3:167-205.
80. Takahashi LK, Turner JG, Kalin NH: Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res 1992;574:131-137.
81. Maccari S, Mormende M, Piazza PV, Simon H, Angelucci L, Le Moal M: Hippocampal type I and type II corticosteroid receptors are modulated by central noradrenergic systems. Psychoneuroendocrinology 1992;17:103-112.
82. Maccari S, Piazza PV, Rouge-Pont F, Angelucci L, Simon H, Le Moal M: Noradrenergic regulation of type-I and type-II glucocorticoid receptors in amygdala and hypothalamus. Brain Res 1992;587:313-318.
83. Yau JLW, Seckl JR: Central 6-hydroxydopamine lesions decrease mineralocorticoid, but not glucocorticoid receptor gene expression in the rat hippocampus. Neurosci Lett 1992;142: 159-162.
84. Fride E, Weinstock M: Increased interhemispheric coupling of the dopamine systems induced by prenatal stress. Brain Res Bull 1987; 18:457-461.
85. Peters DAV: Prenatal stress increases the behavioral response to serotonin agonists and alters open field behavior in the rat. Pharmacol Biochem Behav 1986;25:873-877.
86. Peters DAV: Effects of maternal stress during different gestational periods on the serotonergic system in adult rat offspring. Pharmacol Biochem Behav 1988;31:839-843.
87. Gilad G: The stress-induced response of the septo-hippocampal cholinergic system. A vectorial outcome of psychoneuroendocrinological interactions. Psychoneuroendocrinology 1987; 12:167-184.
88. Imperato A, Puglisi-Allegra S, Casolini P, Angelucci L: Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis. Brain Res 1991;538:111-117.
89. Mark GP, Rada PV, Shors TJ: Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala. Neuroscience 1996;74:767-774.
90. Chrousos GP: Regulation and dysregulation of the hypothalamic-pituitary- adrenal axis: The corticotropin-releasing hormone perspective. Endocr Metab Clin North Am 1992; 21:833-858.
91. Ursin H, Olff M: Psychobiology of coping and defense strategies. Neuropsychobiology 1993; 28:66-71.
92. Charney DS, Redmond Jr DE: Neurobiological mechanisms in human anxiety. Evidence supporting central noradrenergic hyperactivity. Neuropharmacology 1983;22:1531-1536.
93. Robbins TW: Cortical noradrenaline, attention and arousal. Psychol Med 1984;14:13-21.
94. Alonso SJ, Navarro E, Rodriguez M: Permanent dopaminergic alterations in the n. accumbens after prenatal stress. Pharmacol Biochem Behav 1994;49:353-358.
95. Janowsky DS, Overstreet DH, Nurnberger JI Jr: Is cholinergic sensitivity a genetic marker for the affective disorders? Am J Med Genet 1994;54:335-344.
96. Egger GJ, Livesey PJ, Dawason DG: Ontogenetic aspects of central cholinergic involvement in spontaneous alternation behavior. Dev Psychobiol 1973;6:289-299.
97. Sapolsky RM, Krey LC, Mc Ewen BS: Stress down-regulates corticosterone receptors in a site specific manner in the brain. Endocrinology 1984;114:287-292.
98. Takahashi LK: Glucocorticoids and the hippocampus. Developmental interactions facilitating the expression of behavioral inhibition. Mol Neurobiol 1996;13:213-226.
99. Miale IL, Sidman RL: An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 1961;4:227-296.
100. Hoshino K: Histogenic abnormalities of the brain caused by environmental factors: Sensitive period for microcephaly. Congen Anom 1983;23:415-423.
101. Rakic P: Principles of neural cell migration. Experientia 1990;46:882-891.
102. Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N: Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Dev Neurosci 1998;16:209-216.
103. Schmitz C, Bultmann E, Gube M, Korr H: Neuron loss in the mouse hippocampus following prenatal injection of tritiated thymidine or saline. Int J Dev Neurosci 1999;17: 185-190.
104. Amaral DG, Witter MP: The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 1989;31:571-591.
105. Lemaire V, Koehl M, Le Moal M, Abrous DN: Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000;97:11032-11037.
106. West MJ, Slomianka L, Gundersen HJG: Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991;23:482-497.
107. Rasmussen T, Schliemann T, Sorensen JC, Zimmer J, West MJ: Memory impaired aged rats: No loss of principal hippocampal and subicular neurons. Neurobiol Aging 1996;17: 143-147.
108. Lukoyanov NV, Madeira MD, Paula-Barbosa MM: Behavioral and neuroanatomical consequences of chronic ethanol intake and withdrawal. Physiol Behav 1999;66:337-346.
109. Gundersen HJG: Stereology of arbitrary particles. J Microsc 1986;143:3-45.
110. Schmitz C: Variation of fractionator estimates and its prediction. Anat Embryol 1998; 198:371-397.
111. Schmitz C, Hof PR: Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 2000;20: 93-114.
112. Schmitz C, Korr H, Perl DP, Hof PR: Advanced use of 3-D methods for counting neurons. Trends Neurosci 2001;24:377-378.
113. Schmitz C, Korr H, Heinsen H: Design-based counting techniques: The real problems. Trends Neurosci 1999;22:345.
114. Schmitz C: Towards the use of state-of-the-art stereology in experimental gerontology. Exp Gerontol 2000;35:429-431.
115. Schmitz C, Rhodes ME, Bludau M, Kaplan S, Ong P, Ueffing I, Vehoff J, Korr H, Frye CA: Depression: Reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry, in press.
116. Gould E, Gross CG: Neurogenesis in adult mammals: Some progress and problems. J Neurosci 2002;22:619-623.
117. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS: Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 1992;12:3642-3650.
118. Takahashi LK, Turner JG, Kalin NH: Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: Implications for prenatal stress studies. Psychoneuroendocrinology 1998;23:571-581.
119. Ustun TB: Cross-national epidemiology of depression and gender. J Gend Specif Med 2000;3:54-58.
120. Rubin RT, Sekula LK, O'Toole S, Rhodes ME, Czambel RK: Pituitary-adrenal cortical responses to low-dose physostigmine and arginine vasopressin administration in normal women and men. Neuropsychopharmacology 1999;20:434-446.
121. Frye CA, Walff AA: Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav 2002;41:306-315.
122. Jacobs BL, Praag H, Gage FH: Adult brain neurogenesis and psychiatry: A novel theory of depression. Mol Psychiatry 2000;5:262-269.
123. Manji HK, Drevets WC, Charney DS: The cellular neurobiology of depression. Nat Med 2001;7:541-547.
124. Sapolsky RM: Depression, antidepressants, and the shrinking hippocampus. Proc Natl Acad Sci USA 2001;98:12320-12322.
125. Watson JB, Mednick SA, Huttenen M, Wang X: Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 1999;11:457-466.
126. Czéh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M, Bartolomucci A, Fuchs E: Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 2001;98:12796-12801.
127. Joyce JN: The dopamine hypothesis of schizophrenia: Limbic interactions with serotonin and norepinephrine. Psychopharmacology 1993;112:S16-S34.
128. Leonard CM, Kuldau JM, Breier JI, Zuffante PA, Gautier ER, Heron DC, Lavery EM, Packing J, Williams SA, DeBose CA: Cumulative effect of anatomical risk factors for schizophrenia: An MRI study. Biol Psychiatry 1999;46:374-382.
129. Brent RL: Radiation teratogenesis. Teratology 1980;21:281-298.
130. Kimler BF: Prenatal irradiation: A major concern for the developing brain. Int J Radiat Biol 1998;73:423-434.
131. Hicks SP, D'Amato CJ: Effects of ionizing radiation on mammalian development; in Woollam DHM (ed): Advances in Teratology. London, Logos Press, 1966, pp 195-243.
132. Donoso JA, Norton S: The pyramidal neuron in cerebral cortex following prenatal X-irradiation. Neurotoxicology 1982;3:72-84.
133. Bruni JE, Persaud TVN, Hunag W, Froese G: Postnatal development of the rat CNS following in utero exposure to a low dose of ionizing radiation. Exp Toxicol Pathol 1993;45:223-231.
134. Ferrer I: Experimentally induced cortical malformations in rats. Childs Nerv Syst 1993; 9:403-407.
135. Goodhead DT: Initial events in the cellular effects of ionizing radiations: Clustered damage in DNA. Int J Radiat Biol 1994;65:7-17.
136. Wallace SS: Enzymatic processing of radiation-induced free radical damage in DNA. Radiat Res 1998;150:S60-S79.
137. Singh G, Hauswirth WW, Ross WE, Neims AH: A method for assessing damage to mitochondrial DNA caused by radiation and epichlorohydrin. Mol Pharmacol 1985;27: 167-170.
138. Morales A, Miranda M, Sanchez-Reyes A, Biete A, Fernandez-Checa JC: Oxidative damage of mitochondrial and nuclear DNA induced by ionizing radiation in human hepatoblastoma cells. Int J Radiat Oncol Biol Phys 1998;42:191-203.
139. Ames BN, Shigenaga MK, Hagen TM: Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 1993; 90:7915-7922.
140. Korr H, Koeser S, Oldenkott S, Schmidt H, Schultze B: X-ray dose-effect relationship on unscheduled DNA synthesis and spontaneous unscheduled DNA synthesis in mouse brain cells studied in vivo. Radiat Environm Biophys 1989;28:13-26.
141. Korr H, Kurz C, Seidler TO, Sommer D, Schmitz C: Mitochondrial DNA synthesis studied autoradiographically in various cell types in vivo. Braz J Med Biol Res 1998;31: 289-298.
142. May A, Bohr VA: Gene-specific repair of gamma-ray-induced DNA strand breaks in colon cancer cells: No coupling to transcription and no removal from the mitochondrial genome. Biochem Biophys Res Commun 2000;269:433-437.
143. Tang JT, Yamazaki H, Inoue T, Koizumi M, Yoshida K, Ozeki S, Inoue T: Mitochondrial DNA influences radiation sensitivity and induction of apoptosis in human fibroblasts. Anticancer Res 1999;19:4959-4964.
144. Korr H, Rhode HT, Benders J, Dafotakis M, Grolms N, Schmitz C: Neuron loss during early adulthood following prenatal low-dose X-irradiation in the mouse brain. Int J Radiat Biol 2001;77:567-580.
145. Schmitz C, Materne S, Korr H: Cell-type-specific differences in age-related changes of DNA repair in the mouse brain - molecular basis for a new approach to understand the selective neuronal vulnerability in Alzheimer's disease. J Alz Dis 1999;1:387-407.
146. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning. A Laboratory Manual, ed 2. Cold Spring Harbor, Cold Spring Harbor Laboratory Press, 1989.
147. Dikomey E, Franzke J: DNA repair kinetics after exposure to X-irradiation and to internal beta-rays in CHO cells. Radiat Environ Biophys 1986;25:189-194.
148. Kameyama Y, Hoshino K, Hayashi Y: Effects of low-dose X-radiation on the matrix cells in the telencephalon of mouse embryos; in Mahlum DD, Sikow MR, Hackett PL, Andrew FD (eds): Developmental Toxicology of Energy-Related Pollutants. Oak Ridge, US DOE Technical Information Center, 1978, pp 228-236.
149. Hoshino K, Kameyama Y: Developmental-stage-dependent radiosensitivity of neural cells in the ventricular zone of telencephalon in mouse and rat fetuses. Teratology 1988;37: 257-262.
150. Gilmore C, Nowakowski RS, Caviness VS, Herrup K: Cell birth, cell death, cell diversity and DNA breaks: How do they all fit together? Trends Neurosci 2000;23:100-105.
151. Korr H, Philippi V, Helg C, Schiefer J, Graeber MB, Kreutzberg GW: Unscheduled DNA synthesis and mitochondrial DNA synthetic rate following injuring of the facial nerve. Acta Neuropathol 1997;94:557-566.
152. Bandy B, Davison AJ: Mitochondrial mutations may increase oxidative stress: Implications for carcinogenesis and aging? Free Radic Biol Med 1990;8:523-539.
153. Bohr VA, Dianov GL: Oxidative DNA damage processing in nuclear and mitochondrial DNA. Biochimie 1999;81:155-160.
154. Gross NJ, Getz GS, Rabinowitz M: Apparent turnover of mitochondrial deoxyribonucleic acid and mitochondrial phospholipids in the tissues of the rat. J Biol Chem 1969;244: 1552-1562.
155. Menzies RA, Gold PH: The turnover of mitochondria in a variety of tissues of young adult and aged rats. J Biol Chem 1971;246:2425-2429.
156. de Gray ADNJ: A proposed refinement of the mitochondrial free radical theory of aging. Bioessays 1997;19:161-166.
157. Bohr VA, Anson RM: Mitochondrial DNA repair pathways. J Bioenerg Biomembr 1999; 31:391-398.
158. LeDoux SP, Wilson GL: Base excision repair of mitochondrial DNA damage in mammalian cells. Prog Nucleic Acid Res Mol Biol 2001;68:273-284.
159. Lee HC, Yin PH, Lu CY, Chi CW, Wei YH: Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 2000;348:425-432.
160. Wei YH, Lu CY, Lee HC, Pang CY, Ma YS: Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann NY Acad Sci 1998;854:155-170.
161. Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC: Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 1999;96:4820-4825.
162. Kowald A, Kirkwood TBL: A network theory of ageing: The interactions of defective mitochondria, aberrant proteins, free radicals and scavengers in the ageing process. Mutat Res 1999;316:209-236.
163. Schmitz C, Axmacher B, Zunker U, Korr H: Age-related changes of DNA repair and mitochondrial DNA synthesis in the mouse brain. Acta Neuropathol 1999;97:71-81.
164. Norton S: Development of rat telencephalic neurons after prenatal X-irradiation. J Environ Sci Health 1979;C13:121-134.
165. Feldman ML, Dowd C: Aging in rat visual cortex: Light microscopic observations on layer V pyramidal apical dendrites. Anat Rec 1974;178:355.
166. Schmitz C, Grolms N, Hof P, Boehringer R, Glaser J, Korr H: Altered spatial arrangement of layer V pyramidal cells in the mouse brain following prenatal low-dose X-irradiation. A stereological study using a novel three-dimensional analysis method to estimate the nearest neighbor distance distributions of cells in thick sections. Cereb Cortex, in press.
167. Arnold SE, Han LY, Ruscheinsky DD: Further evidence of cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia using spatial point pattern analysis. Biol Psychiatry 1997;42:639-647.
168. Rakic P, Bourgeois JP, Goldman-Rakic PS: Synaptic development of the cerebral cortex: Implications for learning, memory, and mental illness. Prog Brain Res 1994;102:227-243.
169. Rakic P: Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc Natl Acad Sci USA 1995;92: 11323-11327.
170. Rakic P, Lombroso PJ: Development of the cerebral cortex. I. Forming the cortical structure. J Am Acad Child Adolesc Psychiatry 1998;37:116-117.
171. Roper SN: In utero irradiation of rats as a model of human cerebrocortical dysgenesis: A review. Epilepsy Res 1998;32:63-74.
172. Haydar TF, Kuan CY, Flavell RA, Rakic P: The role of cell death in regulating the size and shape of the mammalian forebrain. Cereb Cortex 1999;9:621-626.
173. Rorke LB: A perspective: The role of disordered genetic control of neurogenesis in the pathogenesis of migration disorders. J Neuropathol Exp Neurol 1994;53:105-117.
174. Shimada M, Yamano T, Nakamura T, Morikawa Y, Kusunoki T: Effect of maternal malnutrition on matrix cell proliferation in the cerebrum of the mouse embryo: An autoradiographic study. Pediatr Res 1977;11:728-732.
175. Fushiki S, Hyodo-Taguchi Y, Kinoshita C, Ishikawa Y, Hirobe T: Short- and long-term effects of low-dose prenatal X-irradiation in mouse cerebral cortex, with special reference to neuronal migration. Acta Neuropathol 1997;93:443-449.
176. Hyodo-Taguchi Y, Fushiki S, Kinoshita C, Ishikawa Y, Hirobe T: Effects of continuous low-dose prenatal irradiation on neuronal migration in mouse cerebral cortex. J Radiat Res 1997;38:87-94.
177. Copp AJ, Harding BN: Neuronal migration disorders in humans and in mouse models - an overview. Epilepsy Res 1999;36:133-141.
178. Rubenstein JLR, Rakic P: Genetic control of cortical development. Cereb Cortex 1999;9: 521-523.
179. Gleeson JG, Walsh CA: Neuronal migration disorders: From genetic diseases to developmental mechanisms. Trends Neurosci 2000; 23:352-359.
180. ten Donkelaar HJ: Major events in the development of the forebrain. Eur J Morphol 2000; 38:301-308.
181. Ross ME, Walsh CA: Human brain malformations and their lessons for neuronal migration. Annu Rev Neurosci 2001;24:1041-1070.
182. Palmini A, Andermann E, Andermann F: Prenatal events and genetic factors in epileptic patients with neuronal migration disorders. Epilepsia 1994;35:965-973.
183. Andreasen NC: Symptoms, signs, and diagnosis of schizophrenia. Lancet 1995;346:477-481.
184. Braver TS, Barch DM, Cohen JD: Cognition and control in schizophrenia: A computational model of dopamine and prefrontal function. Biol Psychiatry 1999;46:312-328.
185. Plum F: Prospects for research on schizophrenia. 3. Neurophysiology. Neuropathological findings. Neurosci Res Program Bull 1972; 10:384-388.
186. Corsellis JAN: Psychosis of obscure pathology, in Blackwood W, Corsellis JAN (eds): Greenfield's Neuropathology, ed 3. London, Edward Arnold, 1976, pp 903-915.
187. Harrison PJ: The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999;122:593-624.
188. Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, Bullmore ET: Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 2000;157:16-25.
189. Shenton ME, Dickey CC, Frumin M, McCarley RW: A review of MRI findings in schizophrenia. Schizophren Res 2001;49:1-52.
190. Tsuang MT: Schizophrenia: Genes and environment. Biol Psychiat 2000;47:210-220.
191. Tsuang MT, Stone WS, Faraone SV: Genes, environment and schizophrenia. Br J Psychiatry 2001;40:S18-S24.
192. Sawa A, Snyder SH: Schizophrenia: Diverse approaches to a complex disease. Science 2002;296:692-695.
193. Roberts GW: Schizophrenia: A neuropathological perspective. Br J Psychiatry 1991;158: 8-17.
194. Bloom FE: Advancing a neurodevelopmental origin for schizophrenia. Arch Gen Psychiatry 1993;50:224-227.
195. Roberts GW, Royston MC, Weinberger DR: Schizophrenia, in Graham DI, Lantos PL (eds): Greenfield's Neuropathology, ed 6. London, Arnold, 1997, pp 897-929.
196. Murray RM, Lewis SW: Is schizophrenia a neurodevelopmental disorder? Br Med J 1987;295:681-682.
197. Weinberger DR: Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 1987;44: 660-669.
198. Weinberger DR: From neuropathology to neurodevelopment. Lancet 1995;246:552-557.
199. Kovelman JA, Scheibel AB: A Neurohistological correlate of schizophrenia. Biol Psychiatry 1984;19:1601-1621.
200. Jakob H, Beckmann H: Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J Neural Transm 1986;65: 303-236.
201. Arnold SE , Hyman BT, Van Hoesen GW, Damasio AR: Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch Gen Psychiatry 1991;48:625-632.
202. Akbarian S, Bunney WE Jr, Potkin SG, Wigal SB, Hagman JO, Sandman CA, Jones EG: Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry 1993;50:169-177.
203. Akbarian S, Vinuela A, Kim JJ, Potkin SG, Bunney WE Jr, Jones EG: Distorted distribution of nicotinamide-adenine dinucleotide phosphate- diaphorase neurons in temporal lobe of schizophrenics implies anomalous cortical development. Arch Gen Psychiatry 1993;50:178-187.
204. Peres-Garcia CG, Gonzales-Delgado FJ, Suarez-Sola ML, Castro-Fuentes R, Martin-Trujillo JM, Ferres-Torres R, Meyer G: Reelin-immunoreactive neurons in the adult vertebrate pallium. J Chem Neuroanat 2001;21: 41-51.
205. Costa E, Davis J, Grayson DR, Guidotti A, Pappas GD, Pesold C: Dendritic spine hypoplasticity and downregulation of reelin and GABAergic tone in schizophrenia vulnerability. Neurobiol Dis 2001;8:723-742.
206. Costa E, Davis J, Pesold C, Tueting P, Guidotti A: The heterozygote reeler mouse as a model for the development of a new generation of antipsychotics. Curr Opin Pharmacol 2002;2:56-62.
207. Fatemi SH, Earle JA, McMenomy T: Reduction in Reeler immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiat 2000;5:654-663.
208. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG, Uzunov DP, Smalheiser NR, Davis JM, Pandey GN, Pappas GD, Tueting P, Sharma RP, Costa E: A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci USA 1998;95:15718-1523.
209. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR, Impagnatiello F, Pandey G, Pesold C, Sharma R, Uzunov D, Costa E, DiGiorgi Gerevini V: Decrease in reelin and glutamic acid decarboxylase 67 (GAD67) expression in schizophrenia and bipolar disorder: A postmortem brain study. Arch Gen Psychiatry 2000;57:1061-1069.
210. Arnold SE: Neurodevelopmental abnormalities in schizophrenia: Insights from neuropathology. Dev Psychopathol 1999;11:439-456.
211. Darmanto W, Inouye M, Takagishi Y, Ogawa M, Mikoshiba K, Murata Y: Derangement of Purkinje cells in the rat cerebellum following prenatal exposure to X-irradiation: Decreased reelin level is a possible cause. J Neuropathol Exp Neurol 2000;59:251-262.
212. Selemon LD, Goldman-Rakic PS: The reduced neuropil hypothesis: A circuit-based model of schizophrenia. Biol Psychiatry 1999;45:17-25.
213. Selemon LD, Rajkowska G, Goldman-Rakic PS: Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 1995;52:805-818.
214. Rajkowska G, Selemon LD, Goldman-Rakic PS: Neuronal and glial somal size in the prefrontal cortex: A postmortem study of schizophrenia and Huntington's disease. Arch Gen Psychiatry 1998;55:215-224.
215. Pierri JN, Volk CLE, Auh S, Sampson A, Lewis D: Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry 2001;58:466-473.
216. Fukui Y, Hoshino K, Hayasaka I, Inouye M, Kameyama Y: Developmental disturbance of rat cerebral cortex following prenatal low-dose gamma-irradiation: A quantitative study. Exp Neurol 1991;112:292-298.
217. Ochiai H, Miyahara S, Wakisaka S: Developmental abnormalities of corticospinal tract neurons in prenatally irradiated rats: A study using retrograde labeling with Fast blue and intracellular Lucifer yellow staining. Brain Res 1993;603:129-133.